FY2021 Annual Report

Biodiversity and Biocomplexity Unit
Professor Evan Economo

 

Abstract

Our lab seeks to understand how ecological and evolutionary processes interact to generate and regulate biodiversity across spatiotemporal scales and levels of biological organization.  Living systems are diverse from gene sequences to organismal morphology to communities and ecosystems.  Our goal as biologists is not just to document and catalogue this diversity, but understand the complex interactions and dynamics that generate and sustain biological variation.  In FY2021, our research concentrated in five areas; our project on the evolution of the hyperdiverse ant radiations, our Global Ant Biodiversity Informatics (GABI) project which focuses on compiling analyzing global distributions of past and present ant biodiversity, the systematics, ecology, and evolution of Indo-Pacific ant faunas, the OKEON Churamori Project, and analyzing the evolution of organismal design using x-ray imaging.

1. Staff

  • Dr. Dan Warren, Staff Scientist
  • Dr. Francisco Hita Garcia, Staff Scientist
  • Dr. Larisa Kiseleva, Staff Scientist
  • Dr. Alexandre Casadei Ferreira, Postdoctoral Scholar
  • Dr. Jamie Kass, JSPS Postdoctoral Fellow
  • Dr. Nurit Eliash, Postdoctoral Scholar
  • Fumika Azuma, Research Unit Technician
  • Dr. Kosmas Deligkaris, Research Unit Technician
  • Miyuki Suenaga, Research Unit Technician
  • Yuka Suzuki, Graduate Student
  • Yazmin Zurita-Gutierrez, Graduate Student
  • Julian Katzke, Graduate Student
  • Evropi Toulkeridou, Graduate Student
  • Aibekova Lazzat, Graduate Student
  • Gaurav Agavekar, Graduate Student
  • Shubham Gautam, Graduate Student
  • Chisa Oshiro, Research Unit Administrator

 

2. Activities and Findings

2.1 Global Ant Biodiversity Informatics (GABI) Project

Our understanding of large-scale biodiversity patterns has recently increased dramatically, but available information is strongly biased towards a few groups of vertebrates and plants. Biodiversity patterns in invertebrates, such as insects, are poorly documented despite representing the large majority of species. To address this gap in our knowledge, the Global Ant Biodiversity Informatics (GABI) project has compiled over 250 years of ant research into a single database providing distribution information for all ant species. These data can be used to support all kinds of research and are being used somehow in most of our ant projects. However, the two main analyses we are working on with these data are analyzing global ant diversification patterns across the globe, and a comparison of how global patterns of ant endemism compare with vertebrate groups.  In FY2021, we have continued to maintain and build the GABI dataset so it can be used for different research purposes.  We have published a number of manuscripts based on different aspects of ant biogeography (e.g. La Richelière et al. 2022, Silva et al. 2022, Takashina et al. 2021). We continued and expanded a major georeferencing effort to increase the number of geolocated occurrence points available, and developed a range-mapping pipeline.  We submitted a manuscript that will introduce a new global dataset and models of global ant richness and rarity, and it will be published in the next fiscal year.

2.2 Evolution, Ecology, and Systematics of Hyperdiverse Ant Radiations

Over evolutionary time lineages evolve in and out of ecological niches, evolve through morphological spaces, and ranges expand and contract in geographic space. These transitions may not be independent, some phenotypes may be better suited to certain ecological habitats, some habitats may promote dispersal and colonization, and colonization of new geographic areas may lead to ecological niche shifts. These forces and constraints shape diversification on global and regional scales, but to understand them we need large scale integrated analyses of highly diverse groups.  We have projects analyzing the diversification of several hyperdiverse ant radiations, namely the genera Pheidole, Strumigenys, and Tetramorium.  Pheidole is a hyperdiverse and ecologically generalist group that dominates communities around the tropics.  We have analyzed their global diversification, morphological evolution, and community assembly on islands. Strumigenys is a leaf-litter predator that has evolved a complex trap-jaw mechanism, and we are examining the evolution of this trait in time and space.  In Tetramorium, we are analyzing biogeography, morphological evolution, and transitions between ecological generalism and specialism. 

With phylogenies completed and published for Strumigenys and Pheidole in the previous fiscal year, in FY2021 we made projects on using that data to pursue comparative projects. We published collaborative papers on Pheidole  (Klunk et al.2021, Casadei-Ferreira et al. 2021), have worked on Strumigenys comparative genomics and biomechanics, and made further steps toward finishing the global Tetramorium phylogeny and analyzing biogeographic and patterns of trait evolution.

2.3 Analyzing evolution of organismal design with X-ray micro-CT

Since the earliest biological studies, description and quantification of biological structures has been a basic goal of biology as well as a first step toward deeper understanding of ecological and evolutionary processes.  In Entomology, the primary imaging tools have traditionally been optical microscopy and SEM, which are essential for certain tasks and allow us to see complex structures well. But these are limited in our ability to quantitatively characterize complex shapes, surfaces, and textures.  X-Ray CT has the potential to complement existing tools by providing a digital 3D image of the interior and exterior of the organism.  These images can be manipulated, dissected, measured, and quantified.  We have been developing imaging and post-processing techniques to better quantify the functional morphology of ants, including both external and internal structures. This provides a basis for a research program analyzing the evolution of organismal design. 

In FY2021, we published a number of papers investigating the evolution and diversification of morphology. First, PhD student Lazzat Aibekova published an analysis of ant thoracic anatomy that provides the basis for a broader comparative study on ant locomotory morphology (Aibekova et al. 2022).  Julian Katzke, another PhD student, presented an open source workflow for characterizing muscle architecture from micro-CT data (Katzke et al. 2022), which should be useful for studying a wide range of animals from ants to vertebrates.  We also analyzed a 100-million year old fossil ant that had an amazingly preserved brain (Boudinot et al. 2022), analyzed the bite mechanics of Pheidole (Klunk et al. 2021), and characterized the head anatomy and mandible functional morphology of the rare ant Protanilla (Richter et al. 2021).

2.4 OKEON Churamori Project

In collaboration with other researchers OIST, in FY2013 we initiated a major initiative called the OKEON Chura-Mori Project (OKEON stands for Okinawa Environmental Observation Network).  The goal is to develop an observation system to measure and monitor the environment of Okinawa, in collaboration with the people of Okinawa.  The primary scientific goal is to develop long-term space-time data series from sites across the island.

The field network is now fully operational and collecting data every 2 weeks.  We have also been broadening the activities and partners, we now have over 140 partners in the project.  See the OKEON website for more on our activities. 

In FY2021, we have focused on analyzing 2-year dataset of biweekly ant community changes across our sampling network and are now preparing a manuscript led by Jamie Kass.  We continued a Pacific-wide collaboration with colleagues in the US (Rosemary Gillespie, George Roderick, Haldre Rogers) and Germany (Henrik Krehenwinkel) to deploy metabarcoding methods in Okinawa and across the Pacific islands, and published our first manuscript (Kennedy et al. 2022). 

We continued to participate in ant surveillance research in Japan, with the species arriving to many ports across the country.  We continue to work on our Ministry of Environment research grant for fire ant countermeasures, in collaboration with colleagues in Japan.  In FY2021 we continued to refine pipelines in in our molecular lab, and are conducting experiments on metabarcoding protocols for invasive species detection.  Our preliminary data are promising for this purpose.  Related to this, our collaboration received a major grant from the SERDP program (US DoD) to develop invasive species detection methods for arthropods. 

2.5 Biodiversity Theory

Ecological and evolutionary processes often occur in a spatially complex environment, whether it is an archipelago of islands, patches of forest in a fragmented landscape, or a system of streams in a watershed.  This spatial structure appears on scales of meters to the sizes and arrangements of continents and interacts with biological processes on all of these scales.  Network theory offers a tool for representing the complex patterns of connectivity between ecosystems.  Our work is focused on how the structure of these networks interact with biodiversity dynamics, and how their widespread deconstruction by humans may affect biodiversity.  We also have interest in other areas of theoretical ecology and evolution, and have recently been focusing on increased connections of population genetic and ecological theory with regards to community dynamics.

In FY2021, PhD student Yuka Suzuki continued her investigations of metacommunity dynamcis in spatial dispersal networks, even as she graduated with her PhD. After paper about how network topology controls the transition from species sorting to mass effects (Suzuki & Economo 2021), she is also working on an analysis of how spatial structure promotes or depresses metacommunity stability and has submitted a manuscript.  Postdoctoral fellow Nao Takashina also published a paper on species range size distribution dynamics (Takashina & Economo 2022).

 

3. Publications

3.1 Journals

  1. Takashina, N., Plank, M.J., Jenkins, C. N., Economo, E. P. (2022). Species-range-size distributions: Integrating the effects of speciation, transformation, and extinction. Ecology and Evolution.
  2. Frédérique La Richelière, Muñoz, G., Guénard, B., Dunn, R.R., Economo, E.P., Powell, S., Sanders, N.J., Weiser, M.D., Abouheif, E., Lessard, J.-P. (2022) Warm and arid regions of the world are hotspots of superorganism complexity. Proceedings of the Royal Society B 289.
  3. Silva, R….(203 authors including Casadei-Ferreira, A., Economo, E.P.)…Ribiero, M.A. (2021) ATLANTIC ANTS: a dataset of ants in Atlantic Forests of South America. Ecology 103: e03580.
  4. Beutel, R., Friedrich, F., Economo, E.P. (2021). Patterns of morphological simplification and innovation in the megadiverse Holometabola (Insecta). Cladistics.
  5. Katzke, J., Puchenkov, P., Stark, H., Economo, E.P. (2022) A roadmap to reconstructing muscle architecture from micro-CT data. Integrative Organismal Biology.
  6. Aibekova, L., Beutel, R. G., Richter, A., Keller, R. A., Hita Garcia, F., Economo, E.P. (2022) The skeletomuscular system of workers of the generalized ant genus Formica (Formicidae). Insect Systematics and Diversity.
  7. Boudinot, B., Richter, A., Katzke, J., Keller, R., Economo, E.P., Beutel, R., Yamamoto, S. (2022) Evidence for the evolution of eusociality in stem ants and a systematic revision of †Gerontoformica (Hymenoptera, Formicidae). Zoological Journal of the Linnean Society.
  8. Klunk, C.L., Argenta, M.A., Casadei-Ferreira, A., Economo, E.P., Pie, M.R. (2021) Mandibular morphology, task specialization, and bite mechanics in Pheidole ants (Hymenoptera: Formicidae). Journal of the Royal Society Interface 18: 179.
  9. Richter, A., Keller, R.A., Hita Garcia, F., Billen, J., Katzke, J., Boudinot, B.E., Economo, E.P., Beutel, R.G. (2021) The head anatomy of Protanilla lini (Hymenoptera: Formicidae: Leptanillinae), with a hypothesis of their mandibular movement. Myrmecological News 31: 85-114.
  10. Townsend Peterson, A. et al., (43 authors including Kass, J.M., Warren, D.L.) (2022). ENM2020: A Free Online Course and Set of Resources on Modeling Species' Niches and Distributions. Biodiversity Informatics 17 (2022).
  11. Saeedi, H., Warren, D.L., Brandt, A. (2022). The Environmental Drivers of Benthic Fauna Diversity and Community Composition. Frontiers in Marine Science.
  12. Sigler, K., Warren, D. L., Tracy, B., Forrestel, E., Hogue, G., Dornburg, A. (2021) Assessing temporal biases across aggregated historical spatial data: a case study of North Carolina’s freshwater fishes. Ecosphere 12: e03878.
  13. Lamb, A. D., Lippi, C. A., Watkins-Colwell, G. J., Jones, A., Warren, D. L., Iglesias, T. L., Brandley, M. C., Dornburg, A. (2021) Comparing the dietary niche overlap and ecomorphological differences between invasive Hemidactylus mabouia geckos and a native gecko competitor. Ecology and Evolution 11: 18719-18732.
  14. Hofmann, R., Lehmann, T., Warren, D. L., Ruf, I. (2021) The squirrel is in the detail: Anatomy and morphometry of the tail in Sciuromorpha (Rodentia, Mammalia). Journal of Morphology 282: 1659-1682.
  15. Warren, D.L., Eytan, R., I., Dornburg, A., Iglesias, T. L., Brandley, M. C., Wainwright, P. C. (2021) Reevaluating claims of ecological speciation in Halichoeres bivittatus. Ecology and Evolution 11: 11449-11456.
  16. https://onlinelibrary.wiley.com/doi/10.1002/ece3.7936
  17. Baumbach, L., Warren, D. L., Yousefpour, R., Hanewinkel, M. (2021) Climate change may induce connectivity loss and mountaintop extinction in Central American forests. Communications Biology 4:869.
  18. Warren, D. L., Dornburg, A., Zapfe, K., Iglesias, T. L. (2021) The effects of climate change on Australia’s only endemic Pokémon: Measuring bias in species distribution models. Methods in Ecology and Evolution 12: 985-995.
  19. Piquet, J. C., Warren, D. L., Saavedra Bolaños, J. F., Sánchez Rivero, J. M., Gallo-Barneto, R., Cabrera-Pérez, M. Á., Fisher, R. N., Fisher, S. R., Rochester, C. J., Hinds, B., Nogales, M., López-Darias, M. (2021) Could climate change benefit invasive snakes? Modelling the potential distribution of the California Kingsnake in the Canary Islands. Journal of Environmental Management 294: 112917.
  20. Liu, X., Xu, Z., Hita Garcia, F. (2021). Taxonomic review of the ant genus Lordomyrma Emery, 1897 (Hymenoptera, Formicidae) from China, with description of two species and an identification key to the known species of the world. Asian Myrmecology 14: e014007 (1-33).
  21. Owens, H. L., Merow, C., Maitner, B., Kass, J. M., Barve, V., Guralnick, R. P. (2021) occCite: Tools for querying and managing large biodiversity occurrence datasets. Ecography 44: 1228-1235.
  22. Hu, Z. M., Zhang, Q. S., Zhang, J., Kass, J. M., Mammola, S., Fresia, P., Draisma, S. G. A., Assis, J., Jueterbock, A., Yokota, M., Zhang, Z. (2021) Intraspecific genetic variation matters when predicting seagrass distribution under climate change. Molecular Ecology 30: 3840-3855.
  23. Kass, J. M., Muscarella, R., Galante, P. J., Bohl, C. L., Pinilla-Buitrago, G. E., Boria, R. A., Soley‐Guardia, M., Anderson, R. P. (2021) ENMeval 2.0: Redesigned for customizable and reproducible modeling of species’ niches and distributions. Methods in Ecology and Evolution 12: 1602-1608.
  24. Gavrutenko, M., Gerstner, B. E., Kass, J. M., Goodman, S. M., Anderson, R. P. (2021) Temporal matching of occurrence localities and forest cover data helps improve range estimates and predict climate change vulnerabilities. Global Ecology and Conservation 27: e01569.
  25. Kass, J. M., Takashina, N., Friedman, N. R., Kusumoto, B., Blair, M. E. (2022). Idea paper: Improving forecasts of community composition with lightweight biodiversity monitoring across ecological and anthropogenic disturbance gradients. Ecological Research, Early View.
  26. Zhang, Z., Kass, J. M., Mammola, S., Koizumi, I., Xuecao, L., Tanaka, K., Ikeda, K., Suzuki, T., Yokota, M., & Usio, N. (2021). Lineage‐level distribution models lead to more realistic climate change predictions for a threatened crayfish. Diversity and Distributions, 27: 684 – 695.
  27. Kass, J. M., Meenan, S. I., Tinoco, N., Burneo, S. F., & Anderson, R. P. (2021). Improving area of occupancy estimates for parapatric species using distribution models and support vector machines. Ecological Applications, 31: e02228.
  28. Ryo, M., Angelov, B., Mammola, S., Kass, J. M., Benito, B. M., & Hartig, F. (2021). Explainable artificial intelligence enhances the ecological interpretability of black‐box species distribution models. Ecography, 44: 199-205.
  29. Merow, C.; Galante, P. J; Kass, J. M; Aiello-Lammens, M. E; Babich Morrow, C.; Gerstner, B. E, et al. (2022). Operationalizing expert knowledge in species' range estimates using diverse data types. Frontiers of Biogeography.
  30. Casadei-Ferreira, A., Friedman, N.R., Economo, E.P., Pie, M.R., Feitosa, R.M. (2021) Head and mandible shapes are highly integrated yet represent two distinct modules within and among worker sub-castes of the ant genus Pheidole. Ecology & Evolution 11: 6104-6118.
  31. Ross, S.R.P.-J., Suzuki, Y., Kondoh, M., Suzuki, K., Villa Martín, P., Dornelas, M. (2021) Illuminating the intrinsic and extrinsic drivers of ecological stability across scales. Ecological Research 36: 364-378.

3.2 Oral and Poster Presentations

  1. Warren, D.L., Alex Dornburg, Katerina Zapfe, and Teresa Iglesias. The effects of climate change on an Australian endemic Pokémon. The 69th Annual Meeting of the Ecological Society of Japan, Fukuoka, Japan, March 15 (2022).
  2. Hita Garcia, F. Unraveling taxonomy and evolutionary dynamics of a remarkable ant radiation in Madagascar based on next-generation-sequencing and 3D cybertaxonomy. The 69th Annual Meeting of the Ecological Society of Japan, Fukuoka, Japan, March 15 (2022).
  3. Kass, J. M. Challenges for predicting the future of biodiversity (生物多様性の未来予測への挑戦). Suzuki Award Talk, The 69th Annual Meeting of the Ecological Society of Japan, Fukuoka, Japan, March 15 (2022).
  4. Kass, J. M., Yoshida, T., Ogasawara, M., Suwabe, M., Yoshimura, M., Hita Garcia, F., Fischer, G., Dudley, K. L., Donohue, I., Economo, E. P.「森林・撹乱地」勾配に沿った沖縄アリ群集の季節性の減少 (Loss of seasonality in Okinawa ant communities across a gradient of forest to human disturbance). The 69th Annual Meeting of the Ecological Society of Japan, Fukuoka, Japan, March 14 - 18 (2022) (virtual). 
  5. Takashina, N., Kass, J. M., Yoshida, T., Ogasawara, M., Suwabe, M., Yoshimura, M., Hita Garcia, F., Fischer, G., Dudley, K. L., Donohue, I., Economo, E. P. Loss of seasonality across a forest-urban gradient for ant communities in Okinawa. Ecological Society of Japan, Kanto Branch Public Online Symposium: Human-nature systems in ecological studies and ecosystem/resource management (virtual). July 26 (2021).
  6. Kass, J. M., Guénard, B., Jenkins, C., Dudley, K. L., Azuma, F., Fisher, B., Parr, C., Gibb, H., Longino, J. T., Ward, P. S., Chao, A., Shattuck, S., Lubertazzi, D., Weiser, M., Jetz, W., Guralnick, R., Sanders, N., Dunn, R., Economo, E. P. A global map of ant biodiversity, comparisons with vertebrates, and predictions of unknown hotspots. Early Career Biogeography Conference Amsterdam (Online). International Biogeography Society. October 22 – 24 (2021).
  7. Kass, J. M. 沖縄アリ群集の時間変動/種の相互作用を種の分布モデルに配慮する方法 (Temporal variability of Okinawan ant communities / Methods to consider biotic interactions in species distribution models). 横浜国立大学大学院環境情報研究院森章研究室公開セミナー (Yokohama National University Graduate School of Environment and Information Sciences, Akira Mori Research Lab Public Seminar). July 20 (2021).
  8. Kass, J. M. Introduction to SDMs: theory and practice in R: Model evaluation. Sapienza University, Rome, Italy (virtual). June 10 (2021). Organized by Robert Muscarella.
  9. Kass J. M., Donohue, I., Economo, E. P. 土地被覆と季節性が特徴づける沖縄アリ群集の時間変動 (Characterizing the temporal variability of Okinawan ant communities using land cover and seasonality). Ecological Society of Japan 68th Annual Meeting (virtual). March 17 – 21 (2021).
  10. Casadei-Ferreira, A., Camacho, G.P., Franco, W., Lattke, J.E., Feitosa, R.M., Economo, E.P. Evolution of the sting in Ectaheteromorph ants. Hymathon 2021 Virtual Symposium (Online). May 7 (2021).
  11. Casadei-Ferreira, A. A series of fortunate events: the morphological variation of the ant genus Pheidole. Entomological Society of America Annual Meeting (Online). (2021).
  12. Casadei-Ferreira, A., Camacho, G.P., Franco, W., Lattke, J.E., Feitosa, R.M., Economo, E.P. Sting shape variation and its functional implications in Ectaheteromorphs ants. SICB+ (Online). January  (2022).
  13. Casadei-Ferreira, A., Camacho, G.P., Franco, W., Lattke, J.E., Feitosa, R.M., Economo, E.P. Evolution of the stinging apparatus in ants. The 69th Annual Meeting of the Ecological Society of Japan (ESJ69) (Online). March 15 (2022).
  14. Aibekova, L. The evolution of forward jumping ants. EU-IUSSI 2021 Online Symposium series.
  15. Aibekova, L., Keller, R.A., Katzke, J., Narendra, A., Hita Garcia, F., Economo, E.P. The Evolution of Forward Leaping in Ants. SICB+ Virtual 2022, Poster
  16. Katzke, J., Economo, E.P. A limited number of convergently evolved ecomorphs underlie the morphological diversity of ant mandible shapes. SICB+ Virtual 2022 (Online).
  17. Katzke, J. Procedural Diversity: Analysis and visualization of ant mandibles over the course of four years. 3rd Young Researcher Meeting Morphology (Online). (2022).
  18. Gautam, S., McKenzie, S., Yoshida, T., Katzke, J., Hita Garcia, F., Yamamoto, S., Economo, E.P. Evolution of odorant receptor number across major Hymenopteran lineages. SICB+ Virtual 2022 (Online).
  19. Gautam, S., McKenzie, S., Yoshida, T., Katzke, J., Hita Garcia, F., Yamamoto, S., Economo, E.P. Unraveling the evolution of odorant receptor number across social and non-social Hymenoptera. invited talk, The 2nd AsiaEvo Conference, Tokyo Metropolitan University, Japan, August 16-19, 2021
  20. Zurápiti, Y., Kass, J.M., Jones, M.M., Yoshimura, M., Ogasawara, M., Yoshida, T., Hita Garcia, F., Ovaskainen, O., Economo, E.P. Partitioning the environmental and biological components of
  21. community abundance with joint species distribution models. The 69th Annual Meeting of the Ecological Society of Japan, Fukuoka, Japan, March 15 (2022).

3.3 Seminars

  1. Economo, E.P. (2022, February 10) McGill University, Department of Entomology, Spring 2022 Seminar Series. “Global ant diversity: treasure-maps, trap-jaws, and the metaverse”
  2. Economo, E.P. (2022). Texas A&M University, Department of Entomology “The global diversification of ants: treasure-maps, trap-jaws, and the metaverse”
  3. Economo, E.P. (2022, February 14) University of Texas at Austin, Department of Integrative Biology “The global diversification of ants: treasure-maps, trap-jaws, and the metaverse”
  4. Economo, E.P. (2021) City College of New York, Department of Biology “The global diversification of ants: treasure-maps, trap-jaws, and the metaverse”
  5. Economo, E.P. (2021) UMass Lowell, Department of Biology “The global diversification of ants: treasure-maps, trap-jaws, and the metaverse”
  6. Economo, E.P. (2021) Yale University, Department of Ecology and Evolutionary Biology, “The global diversification of ants: treasure-maps, trap-jaws, and the metaverse”
  7. Economo, E.P. (2021) EU-IUSSI annual meeting “The Evolution of Trap-Jaw Mandibles in Ants”
  8. Deligkaris, K. (January 27, 2022). Project management with Jira. OIST Graduate School Mini Course. Japan.
  9. Deligkaris, K. (March 22, 2022). Introduction to Confluence as an academic Wiki. (OIST Tani Unit/Froese Unit)
  10. Kass, J. M. (September, 2021 through present). Japan Eco-Evo English Seminar (monthly). Organized with Mizumoto, N.
  11. Kass, J. M., Ishihama, F., Koide, D. Wallace: 再現可能な種の分布モデリングのためのフレキシブルなプラットフォーム (Wallace: a flexible platform for reproducible species distribution modeling). In Japanese. 
  12. Kass, J.M. (September 27, 30 and October, 4, 2021). Mini Course: R Package Development. Okinawa Institute of Science and Technology Graduate University. 1) Using devtools and roxygen for package development; 2) Unit testing,; 3) Graphical user interfaces with shiny. Other instructors: Ayala R, Plessy C.